Handedness and P300 from Auditory Stimuli
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1 BRAIN AND COGNITION 35, (1997) ARTICLE NO. BR Handedness and P300 from Auditory Stimuli Joel E. Alexander Western Oregon State College and John Polich The Scripps Research Institute The P3(00) event-related potential (ERP) was elicited in 20 left- and 20 righthanded normal young adult male subjects using a simple auditory stimulus discrimination task. P3 amplitude from the target stimuli was larger at anterior electrode sites for left- compared to right-handed subjects. P3 latency from the standard stimuli was shorter for left- compared to right-handers. The N1, P2, and N2 components generally demonstrated similar handedness effects. The relationship of ERP amplitude and handedness to anatomical variables and cognitive factors is discussed Academic Press Hemispheric information processing differences have been demonstrated by using behavioral techniques for auditory, visual, and tactile stimuli (Hellige, 1993; Ivry & Lebby, 1993; O Boyle, van Wyhe-Lawler, & Miller, 1987; Polich, 1993), as well as with electroencephalographic (EEG) measures (Alexander & Sufka, 1993; Alexander, O Boyle, & Benbow, 1996; Davidson, Chapman, Chapman, & Henriques, 1990; Gevins et al., 1979) in a wide vari- Collaborative studies on the Genetics of Alcoholism (H. Begleiter, SUNY HSCB, Principle Investigator; T. Reich, Washington University, Co-Principle Investigator) includes six different centers where data collection takes place. The six sites and Principle Investigator and Co- Investigators are: Indiana University (J. Nurnberger, Jr., P. M. Conneally), University of Iowa (R. Crowe, S. Kuperman), University of California at San Diego and The Scripps Research Institute (M. Schuckit, F. E. Bloom), University of Connecticut (V. Hesselbrock), State University of New, Health Sciences Center at Brooklyn (H. Begleiter, B. Porjesz), and Washington University in St. Louis (T. Reich, C. R. Cloninger). This national collaborative study is supported by the National Institute on Alcohol Abuse and Alcoholism (NIAAA) by U.S.P.H.S. Grants NIAAA U10AA The first author was supported by NIAAA Training Grant AA This paper is publication NP9001 from The Scripps Research Institute. Correspondence and reprint requests should be addressed to J. Polich, Department of Neuropharmacology TPC-10, The Scripps Research Institute, North Torrey Pines Road, La Jolla, CA 92037; polich@scripps.edu /97 $25.00 Copyright 1997 by Academic Press All rights of reproduction in any form reserved.
2 260 ALEXANDER AND POLICH ety of task situations. In addition, despite a general impression that the P3(00) cognitive event-related potential (ERP) is of equal amplitude about the midline (Donchin, Kutas, & McCarthy, 1977), similar hemispheric asymmetries have been observed when task conditions that encourage differential cerebral processing are employed (Kok & Rooyakkers, 1986; Schweinberger & Sommer, 1991; Tenke, Bruder, Towey, Leite, & Sidits, 1993). Moreover, several reports even have found P3 amplitude from normal young adult subjects is greater over the right compared to that over the left cerebral hemisphere in the absence of a specific laterality task when a simple stimulus discrimination paradigm is used to elicit the ERPs (Bruyant, Garcia-Larrea, & Mauguiere, 1993; Holinger et al., 1992; Karniski & Blair, 1989; Naumann et al., 1992). These findings suggest that the P3 component may be innately lateralized because of fundamental neurophysiological differences between the cerebral hemispheres (Alexander et al., 1995, 1996). A major factor that has not been examined in these studies is subject hand preference even though this variable may be of some importance for ERP laterality effects, since handedness is considered to be a behavioral manifestation of individual differences in hemispheric cerebral asymmetry (Halpern, 1992). The relationship of handedness to cerebral lateralization is complex (Braun et al., 1994; Bryden & Steenhuis, 1991; Hardyck & Petrinovich, 1977; McKeever, 1991; Sergent, 1990), but the consistent historical evidence for a 90% preponderance of right-handed preference (Coren & Porac, 1977) and fairly clear indications of genetic determination (Annett, 1985; Carter- Saltzman, 1980) strongly imply that preferential human hand use stems from neuroanatomical causes. In support of this proposition, several neuroanatomy and brain imaging studies have found weaker cerebral size asymmetries for left- compared to right-handed subjects (e.g., Galaburda, LeMay, Kemper, & Geschwind, 1977; LeMay, 1977), although consistent handedness or familial sinistrality effects are not always obtained (cf. Chui & Damasio, 1980; Koff, Naeser, Pieniadz, Foundas, & Levine, 1986). Of importance in this context are observations that corpus callosal size is related directly to handedness preference: Left-handed males have larger callosal areas than right-handed males (Dennenberg, Kertesz, & Cowell, 1991; Habib et al., 1991; Witelson, 1985). Even though there is some debate as to whether these anatomical differences occur primarily at the anterior or posterior sections of the corpus callosum and whether subject sex interacts with callosal size and handedness (cf. Driesen & Raz, 1995; Steinmetz et al., 1992; Weis, Weber, Wenger, & Kimbacher, 1988; Witelson, 1989, 1992), these findings indicate that the neural basis for hand preference is a major factor underlying neurobehavioral (e.g., Christman, 1989; Gordon & Kravetz, 1991; Hines, Chiu, McAdams, Bentler, & Lipcamon, 1992; Polich & Morgan, 1994; Yazgan, Wexler, Kinsbourne, Peterson, & Leckman, 1995) or electrophysiological laterality effects (e.g., Barrett & Rugg, 1989; Kutas, Van Patten, & Besson, 1988; Rugg, 1985).
3 P300 AND HANDEDNESS 261 Given this background and because P3 amplitude has been found to be asymmetric in amplitude across the hemispheres for right-handers, it is not unreasonable to suppose that subject handedness may affect this ERP component. Indeed, since the anatomical origins of subject handedness can contribute to cognitive activity (McKeever, 1991; Polich & Morgan, 1994; Witelson, 1992), handedness also could affect the neural operations underlying P3 generation. Several studies have suggested that multiple generators are engaged when the P3 component is produced (Johnson, 1993; Knight, 1990), with additional findings implying that activation of frontal cortical areas occurs in conjunction with temporal parietal sources (Courchesne, Hillyard, & Galambos, 1975; Knight, Scabini, Woods, & Clayworth, 1989). This view is consistent with positron-emission tomography results that indicate frontal lobe activity reflects initial attentional mechanisms that are necessary for the stimulus discrimination operations that elicit the P3 (Pardo, Fox, & Raichle, 1991; Posner, 1992). Assuming that interhemispheric communication occurs as these processes are activated (Hellige, 1993; Sergent, 1990), it is plausible that the P3 ERP would be larger and perhaps occur earlier over the frontal recording areas in individuals whose corpus callosal connections are larger than in individuals whose callosal connections are not as prominent. Such handedness effects could occur because information transmission from one hemisphere to the other might be facilitated if callosal connections were larger so that component amplitude and latencies at the midline (and other sites) would be affected. The present study was designed to test this hypothesis by determining whether the P3 component from a simple auditory discrimination task is different in left- compared to right-handed males. METHOD Subjects. A total of 20 left- and 20 right-handed, normal young adult males (M 22.6, SD 1.8 years) served as subjects. Handedness was evaluated by a six-item handedness questionnaire (Annett, 1985), with additional items that assessed familial sinistrality. Lefthandedness was defined as having left-hand preferences for a minimum of four of the six tasks (M 5.6, SD.6); right-handedness was defined as showing only right (i.e., no lefthand) preferences for all questions (M.0, SD.0). The mean number of left-handed family members reported by the left-handed subjects was 1.4 (SD.68, mode 1); the mean number of left-handed family members reported by the right-handed subjects was.0. Hence, the sinistral sample was strongly left-handed. All subjects reported an absence of psychiatric or neurologic problems, were screened for alcohol/drug use, and received pecuniary remuneration. Recording conditions and procedure. EEG activity was recorded monopolarly using an electrode-cap at 19 electrode sites (Fp1/2, F3/4, C3/4, P3/4, F7/8, T7/8, P7/8, O1/2, Fz, Cz, Pz) referred to the nose, with a forehead ground and impedances at 5 KΩ or less. Electroocular (EOG) activity was measured with one electrode placed at the outer canthus of the left eye for horizontal eye movement and a second electrode placed on the forehead to monitor vertical eye movements. The filter bandpass was Hz (3 db down, 6 db octave/slope). The EEG was digitized at 3.9 ms/point for 1500 ms, with a 187 ms prestimulus baseline. ERP data were averaged on-line with the same computer also used to control the stimulus presentation and artifact rejection. Trials on which the EEG or EEG exceeded 73.3 µv were rejected automatically.
4 262 ALEXANDER AND POLICH ERPs were elicited with 400 auditory binaurally presented stimuli consisting of 600 Hz (standard) and 1600 Hz (target) tones presented at 60 db SPL (10 ms r/f, 60 ms plateau). The interstimulus interval was 1.5 s and the target tone occurred randomly with a probability of.125. Subjects were instructed to press a key pad with their forefinger whenever a target tone was detected and to refrain from responding to the standard. Response hand was counterbalanced across subjects in both handedness groups. Stimulus presentation ended when the first 25 target and 75 standard artifact-free stimuli were acquired. RESULTS All analyses of variance employed Greenhouse Geisser corrections to the degrees of freedom for the repeated measures factors with at least three levels. Only probability values for the corrected df are reported. Post-hoc mean comparisons were performed using the Newman Keuls procedure. Task Performance Task performance was nearly perfect for both groups, with the total number of errors (misses and false alarms) for left-handers at.3% and righthanders at.4%. Mean response time for the target stimuli was for left-handers 412 ms (SD 52.7) and right-handers 428 ms (SD 51.1), with no reliable difference found (F 1, p.45). Hence, both groups performed the task with virtually no error and comparable response times. Component Measurement and Analyses Waveforms were assessed visually and individually for each subject to identify amplitudes and latencies of the N1, P2, N2, and P3 components at each electrode site by locating the most positive or negative component within the latency windows of , , , and ms, respectively. Amplitude was measured at the peak of the component relative to the mean of the prestimulus baseline, with peak latency defined as the time of maximum positive or negative amplitude within the latency window. Two points should be noted about this approach: (1) These procedures facilitated the measurement of all components from both the target and standard stimuli, even when the potentials were not morphologically robust (e.g., P3 from the standard tones). (2) This method produces individual component measurements that are unrelated to each other an assertion that has been verified empirically (Polich, 1992), since each potential is thought to reflect a different set of information processing events. The grand average ERP waveforms for the target and standard stimuli at each electrode position are illustrated in Fig. 1. The mean amplitude/latency values for the P3 component as a function of lateral electrode position and stimulus type are presented in Fig. 2. Although response hand was counterbalanced across subjects, analysis of this variable revealed no influence on the effects reported below, and it will
5 FIG. 1. Grand average event-related potentials from the target and standard stimuli for leftand right-handed subjects (N 20/handedness group).
6 264 ALEXANDER AND POLICH FIG. 2. Mean P3 amplitude and latency from the target and standard stimuli for left- and right-handed subjects as a function of lateral and anterior-to-posterior electrode sites (LL, left lateral; LM, left medial; C, central; RM, right medial; RL, right lateral). not be considered further. Preliminary analyses indicated no reliable handedness effects from the Fp1/2 and O1/2 electrode sites, and these will not be considered further. All other statistical analyses used the anterior-to-posterior (frontal, central, parietal), lateral (F7/8, T7/8, P7/8), medial (F3/4, C3/4, P3/ 4), and central (Fz, Cz, Pz) electrode locations. Separate three-factor (handedness group anterior-to-posterior electrode lateral electrode location)
7 P300 AND HANDEDNESS 265 analyses of variance were performed on the amplitude and latency data obtained from each of the stimulus types for each component. Because the anterior-to-posterior and lateral electrode factors produced main effects in the typical directions for each component, these variables will receive comment only if they yielded statistically reliable interactions with subject handedness. P3 Component Target stimulus P3 amplitude was larger for left-handers across the anterior locations compared to right-handers who demonstrated larger component amplitudes at the posterior locations, as indicated by a significant interaction between the handedness group and anterior-to-posterior electrode factors, F(2, 76) 5.3, p.02. The reliability of this effect is supported by the observation that 17 of 20 left-handed subjects demonstrated this amplitude pattern; the 3 other subjects generally evinced frontal amplitudes midway between or similar to the right-handed subjects. In addition, P3 latency from the standard stimuli was shorter for left- compared to right-handers, F(1, 38) 9.6, p.01. Further, the degree to which the handedness contributed to P3 amplitude in the absence of any overall differences between the left- and right-handed subjects was assessed by normalizing all values into a percentage based on the Pz electrode site measures (cf. Johnson, 1993). Analysis of these data produced the same outcome for P3 amplitude from the target stimuli, with a somewhat stronger effect obtained (p.01). N1, P2, and N2 Components Analyses of the N1, P2, and N2 components were conducted in the same fashion (normalizing transformations for these components has not been demonstrated and will not be considered here). N1 amplitude did not differ between left- and right-handed subjects. N1 latency from the standard stimuli was shorter for left- compared to right-handed subjects, F(1, 38) 4.5, p.05, most notably at lateral electrode locations, F(4, 152) 8.4, p.001 an observation confirmed by post-hoc assessments (p.001). P2 amplitude from the standard stimuli was smaller for the left- compared to right-handers, more so at the central and over the left hemisphere to yield a complex interaction between handedness group and lateral location factors, F(4, 152) 4.3, p.005. Although P2 latency from the standard stimuli was shorter for the left- compared to the right-handed group, F(1, 38) 4.8, p.05, inspection of the individual data points revealed that this outcome occurred because of the influence of a few left-handed subjects who produced very short latencies. N2 amplitude did not produce any reliable handedness effects. N2 latency was shorter at anterior locations for left- compared to right-handers for the target stimulus, F(2, 76) 3.5, p.05. Posthoc analysis indicated that this difference originated primarily from the ante-
8 266 ALEXANDER AND POLICH rior electrodes (p.01). Overall, the N1, P2, and N2 components tended to mimic the handedness effects observed for the P3, with left-handed subjects producing larger amplitudes and shorter latencies compared to right handed subjects. Although P2 amplitude from the standard stimuli was smaller for the left- relative to right-handed subjects, this result stemmed from an interaction between handedness group and both the anterior-to-posterior as well as the lateral electrode locations. Thus, with this one exception, the significant ERP effects were larger amplitudes and shorter in latencies for the leftrelative to the right-handed subjects. DISCUSSION P3 amplitude from the target stimuli was reliably larger for left- compared to right-handed subjects at the anterior electrode positions, with right-handed subjects demonstrating larger amplitudes than left-handed subjects at the posterior electrode positions. These outcomes were obtained even when overall handedness group effects were adjusted with normalizing procedures. P3 latency from the standard stimuli also was shorter for left- compared to right-handed subjects. The N1, P2, and N2 components generally produced results similar to those observed for the P3. The source of handedness effects on ERPs is not known. It may be that brain morphology, skull thickness, or cranial differences between handedness groups contributed to the P3 effects, since these factors can affect ERP amplitude (e.g., Daniel, Myslobodsky, Ingraham, Coppola, & Weinberger, 1989). Variation in the underlying neural mass could then influence electrophysiological measures by redirecting current flow through the skull, such that larger amplitudes are recorded over locations containing more cellular volume and/or having thinner skull widths (cf. Donchin, Karis, Bashore, Coles, & Gratton, 1986). Although a plausible explanation, measurable cranial irregularities (e.g., plagiocephaly) occur only in about 10% of the population (Binnie, Dekkerm, Smit, & Van der Linden, 1982) and yield slight and apparently unstable relationships between skull thickness and occipital EEG alpha asymmetry (Chui & Damasio, 1980; Myslobodsky et al., 1989). Since the P3 handedness effects occurred primarily between the frontal and parietal locations, and because it is difficult to associate cranial structural differences to the latency effects, it is likely that the present findings are unrelated to skull and brain morphology variation. Given the previously reported explicit anatomical differences between left- and right-handed individuals with respect to corpus callosal size (Dennenberg et al., 1991; Driesen & Raz, 1995; Habib et al., 1991; Witelson, 1985, 1989), it is not unreasonable to suppose that ERP measures might be influenced by variation in callosal mass between the strongly left- and righthanded male subjects employed in the present study (cf. Steinmetz et al., 1992; Weis et al., 1988; Witelson, 1992). If the size of the callosal connection
9 P300 AND HANDEDNESS 267 does contribute to communication efficiency between the hemispheres, variation in P3 values between handedness and, therefore, callosal groups may be reflecting related differences in information processing capability. Although an intriguing possibility, the exact nature of these ERP/handedness differences is still unclear because they could originate from either (1) a difference in neural processing efficiency related to callosal size i.e., larger amplitudes and shorter latencies with larger callosal cross-sections, or (2) real variation in cognitive function in terms of where, when, and how P3 attentional/memory operations are performed. However, assuming that task processing is communicated via the corpus callosum, discriminating the target from a standard stimulus could initiate frontal lobe engagement, because such a process requires the consistent application of attentional focus (Pardo et al., 1991; Posner, 1992). In this view, left- and right-handed subjects may differ with respect to how the output of fundamental discrimination processes are propagated through the cortical areas involved in P3 generation. The generally similar handedness findings for the preceding sensory ERPs also support this conclusion, as do the indications of hemispheric amplitude asymmetry found for both groups at the frontal electrode sites (cf. Alexander et al., 1995, 1996). A major theory of the P3 posits that this ERP component reflects a developing representation within short-term memory (Donchin & Coles, 1988; Donchin et al., 1986). This hypothesis is supported by findings from human lesion studies suggesting that multiple neural generators are involved in P3 production (Johnson, 1993; Knight et al., 1989; Yamaguchi & Knight, 1990). In addition, a strong alerting stimulus will elicit an earlier P3a subcomponent that is generally largest over a frontal/central electrode sites (cf. Courchesne et al., 1975; Katayama & Polich, 1997; Squires, Squires, & Hillyard, 1975) and indicates initial signal evaluation (Ford et al., 1994; Knight, 1990), with subsequent attentional capacity and memory processes indexed by the central/parietal or canonical P3b (Knight et al., 1989; Picton, 1992; Polich & Squire, 1993). Because the obtained P3 amplitude handedness results were the most reliable for the target stimulus, directed attention may contribute specifically to these handedness effects. Thus, the frontal parietal P3 differences observed between the left- and right-handed subjects could reflect subject group neurocognitive variation for the processes activated during oddball task performance. REFERENCES Alexander, J., & Sufka, K Cerebral lateralization in homosexual males: A preliminary EEG investigation. International Journal of Psychophysiology, 15, Alexander, J., O Boyle, M. W., & Benbow, C. P Developmental advanced EEG alpha power in gifted male and female adolescents. International Journal of Psychophysiology, 23, Alexander, J., Bauer, L., Kuperman, S., Rohrbaugh, J., Morzorati, S., O Connor, S., Porjesz,
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